Discussion
Ecosystem processes interact via exerting trade-offs or legacy effects
(Reich 2014). Disentangling the linkages among processes could improve
the predictive and mechanistic understanding of nutrient-cycling
responses to changing environments (Cornwell et al. 2008). For the first
time, we integrated the vertical (belowground nutrient absorption vs
aboveground nutrient resorption) and temporal processes (nutrient flows
from green leaf to senesced leaf to leaf litter) associated with the
whole-plant nutrient economy among 15 subtropical tree species.
Nutrients in new leaves are from two pathways: root absorption from soil
(‘Get’) and resorption from senesced leaves (‘Save’) (Wright & Westoby
2003). We found that root nutrient absorption potential was negatively
correlated with leaf nutrient resorption proficiency (Fig. 2a),
indicating a cost-benefit trade-off between belowground absorption and
aboveground resorption in nutrient acquisition pathways (Wright &
Westoby 2003). Such an economic trade-off has further caused a legacy
effect on subsequent leaf-litter decomposition (‘Return’) as indicated
by the negative relationship between nutrient resorption proficiency and
mass loss rate (Fig. 2a). The active trade-off between absorption and
resorption as well as the passive trade-off between resorption and
decomposition jointly indicate the existence of the ‘GSR’ continuum.
The continuum centred primarily on the P economy when examining the
specific nutrients. The PAP was negatively correlated with PRP (P= 0.048; Fig. 2a), indicating that greater root nutrient absorption can
lead to an increased P concentration in leaf litter (i.e. decreased
PRP). Meanwhile, P concentration in leaf litter was positively
correlated (i.e. PRP was negatively correlated) with the decomposition
rate (P = 0.035; Fig. 2a). The resorption proficiency rather than
efficiency that emerged in these linkages supports the argument that
selection acts upon the residual nutrient concentration in senesced
leaves rather than proportional resorption per se (Killingbeck
1996; Wright & Westoby 2003). The allocation of effort toward nutrient
absorption and resorption depends on both soil nutrient availability and
the cost involved in these processes
(Kou et al. 2017). The
continuity of the P economy could be related to the local edaphic
conditions, where soil P availability (6.54 mg kg-1;
Table S3) is relatively low compared to the global level (Zhu et
al. 2016). For example, lower P availability can enhance root
nutrient foraging strategies (Kou et al. 2018b; Li et al. 2019)
and retard leaf-litter decomposition (Jiang et al. 2018, 2019) in
P-deficient subtropical forests. Considering that nutrients obtained via
resorption also incur a cost, e.g. the hydrolysis of organic compounds
(Norby et al. 2000), plants should make an active trade-off between
nutrient acquisition pathways by decreasing P resorption (i.e. saving
less nutrients) for cost saving.
These processes associated with the N economy were not well linked, as
indicated by the decoupling between NAP and NRP (P >
0.05; Fig. 2a). The discontinuity in the N economy supports our
hypothesis that the continuum is mainly determined by the trade-off
between the two nutrient acquisition pathways. The trade-off
disappearance was possibly because N may not be the most limiting
nutrient in N-rich subtropical soils (Kou et al. 2018a). The
discontinuity may alternatively be related to the diverse forms of N.
Unlike P, which is exported in inorganic form (Vance et al. 2003), N can
be exported in a diverse array of inorganic and organic forms
(Takebayashi et al. 2010). In contrast to ammonium, which must be
assimilated in roots, nitrate can be absorbed into organic compounds in
roots and leaves (Wang & Macko 2011; Zhou et al. 2020). The dual
pathways of nitrate assimilation might influence the assessment of root
absorption and leaf resorption, obscuring their linkages. Like the P
economy, NRP was marginally negatively correlated with decomposition
rate (P = 0.052; Fig. 2a), consistent with a recent study showing
linkages between leaf nutrient resorption and litter decomposition (Xu
et al. 2020). This is unsurprising because the initial nutrient
chemistry of leaf litter is closely associated with resorption (Deng et
al. 2018) and inherently determines decomposition rates at the local
scale (Cornwell et al. 2008).
The continuum conformed to the economics spectrum theory, when linking
LES to ‘GSR’ continuum (Fig. 4). The one-dimensional ‘fast-slow’ LES,
capturing a suite of key traits, represents species strategies as shaped
by their evolutionary history (Reich et al. 1997; Wright et al. 2004)
and assumes that the acquisitive-strategy species live fast and die
young, while the conservative-strategy species live slow and steady
(Wright et al. 2004). We correlated the PC1 scores on the LES with these
processes, and found that species at the fast end of the spectrum had
higher PAP (R 2 = 0.27, P = 0.047; Fig.
4a) and litter P concentration (R 2 = 0.50,P = 0.003; Fig. 4b), while species at the slow end presented the
opposite patterns. These results indicate that species at both ends of
the LES have contrasting investment strategies regarding nutrient
acquisition: acquisitive-strategy species rely more on nutrient
absorption but less on nutrient resorption compared to the
conservative-strategy species. Less resorption for the
acquisitive-strategy species yielded higher-quality leaf litter, and
thus faster decomposition (R 2 = 0.39, P= 0.013; Fig. 4c). Such a passive trade-off implies that
selection acts not only upon
resorption but also upon decomposability by influencing the residual
nutrient concentration in senesced leaves. These findings jointly
suggest that the trait-based LES can be extrapolated to the
process-based ‘GSR’ continuum.
Nutrient return via decomposition provides feedback to the soil matrix
and may, in turn, influence root absorption. Perennial plants colonising
a habitat may deploy nutrient foraging strategies in multiple
dimensions, such as the ‘afterlife’ strategy—decomposition. Based on
root trait-decomposition linkages, we found that the
acquisitive-strategy species have thinner absorptive roots, but slower
root decomposition compared to the conservative-strategy species (Jiang
et al. 2021). This finding suggests a potential trade-off between
absorptive-root turnover (diameter as a proxy) and decomposition and a
possible belowground mechanism underlying species coexistence (Jiang et
al. 2021). Despite this, there was no direct link between root
absorption and leaf-litter decomposition on the ‘GSR’ continuum
(P > 0.05; Fig. S3), implying that fast
decomposition may not enable the acquisitive-strategy species to preempt
the returned nutrients. This asymmetry could be related to two causes.
First, leaf litter can decompose away from the home field under physical
forces from wind or forest animals (Veen et al. 2019). Second, soil
microorganisms or neighbouring plants may compete for and immobilise the
returned nutrients (Barbe et al. 2017), which impels the
acquisitive-strategy species to run steadily in a fast lane.
The ‘GSR’ continuum running on P economy emerged among ECM species
rather than AM species (Fig. 4), supporting our hypothesis that the
continuum varied with mycorrhizal type. The contrasting patterns between
mycorrhizal types could be because ECM species generally dominate in
‘slow-cycling’ ecosystems with nutrient conservative traits, while AM
species dominate ‘fast-cycling’ ecosystems with nutrient acquisitive
traits (Philips et al. 2013). Compared to AM species, ECM species may
have a strict budget for C investment and thus a tight linkage between
root absorption and leaf resorption. Furthermore, AM and ECM species
have different degrees of dependence on mycorrhizal fungi based on the
root-fungal collaboration gradient globally (Bergmann et al. 2020). From
absorptive-root trait comparisons between AM and ECM species, we found
that ECM species had greater BI and SRL (marginally significant), and AM
species had higher RD (Table 1). These divergences in root traits
implied that AM species rely more on mycorrhizal symbiosis, while ECM
species rely more on roots themselves when acquiring the limiting
nutrients (Bergmann et al. 2020). Therefore, the two pathways of
nutrient acquisition could be coupled for the more self-dependent ECM
species compared to the more symbiosis-dependent AM species.
While leaf nutrient resorption and leaf-litter decomposition are
negatively correlated (Xu et al. 2020), it remains unclear whether the
trade-off between the two processes depends on the mycorrhizal type. By
partitioning all species into two mycorrhizal groups, we found a tight
linkage between these two processes among ECM species (P = 0.022;
Fig. 2c) rather than AM species (P > 0.05; Fig. 2b).
This divergent pattern may be related to the contrasting trait controls
over leaf-litter decomposition in AM and ECM species (Phillips et al.
2013). Leaf-litter decomposition of ECM species was associated more
closely with chemical traits (N and P) (Table S4). In contrast,
decomposition of AM species was more correlated with morphological
traits (e.g. SLA and LTD; Table S4) rather than chemical traits,
although the ‘fast-slow’ LES was linked to decomposition in AM species
(Fig. 4c). Despite these findings, the limited number of species makes
it difficult to draw robust conclusions when taking a closer look at the
mycorrhizal type, although AM (n = 8) and ECM (n = 7)
species were comparable in terms of sample size. Studies incorporating
more mycorrhizal tree species are therefore needed to further examine
these active and passive trade-offs between nutrient-associated
processes.
Overall, our results suggest that there was an active trade-off between
root P absorption and leaf P resorption, which caused a passive
trade-off between leaf P resorption and leaf-litter decomposition. Based
on these findings, we conclude that the ‘GSR’ continuum exists and runs
on the P economy among these subtropical tree species, providing a
predictive framework for the whole-plant nutrient economy. Importantly,
we linked the ‘fast-slow’ leaf economics spectrum to the processes
associated with tree nutrient economy on this continuum and revealed
that species with acquisitive leaf traits have greater root P
absorption, lower leaf P resorption, and faster leaf-litter
decomposition, while species with conservative leaf traits presented
opposite patterns. These findings imply that the ‘fast-slow’ leaf
economics spectrum can be extended to the process-based ‘GSR’ continuum
and advance our understanding of the adaptive strategies of acquisitive
and conservative species at multi-dimensional scales. Furthermore, the
‘GSR’ continuum emerged among ECM species rather than AM species,
demonstrating the importance of mycorrhizal symbiosis in regulating the
tree nutrient economy.